Asian-Australasian Journal of Animal Sciences

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
권호 표지
DOI QR코드

DOI QR Code

Investigation of the Insulin-like Growth Factor System in Breast Muscle during Embryonic and Postnatal Development in Langshan and Arbor Acres Chickens Subjected to Different Feeding Regimens

  • Lu, F.Z. (College of Animal Science and Technology, Nanjing Agricultural University,Zhejiang Academy of Agricultural Sciences) ;
  • Chen, J. (College of Animal Science and Technology, Nanjing Agricultural University) ;
  • Wang, X.X. (College of Animal Science and Technology, Nanjing Agricultural University) ;
  • Liu, Honglin (College of Animal Science and Technology, Nanjing Agricultural University)
  • Received : 2008.04.19
  • Accepted : 2008.09.02
  • Published : 2009.04.01
Download PDF
⟨ Previous Next ⟩

Abstract

Nutrient availability may control muscle growth directly and indirectly through its influence on regulatory factors. We analyzed the effects of nutrient availability on the breast muscle insulin-like growth factor system. Real time RT-PCR was used to quantify the level of transcription in breast muscle from Langshan (LS) layer and Arbor Acres (AA) broiler chickens subjected to different feeding regimens during embryonic and postnatal development. The AA chickens were fed AA diet (AA, control group) while the LS chickens were either fed LS diet (LL) or AA diet (LA). According to our results, insulin-like growth factor (IGF)-II (embryonic day 16 (E16) - postnatal day 42 (P42)), IGF-I receptor (IGF-IR, E18-P42), and IGF binding protein (IGFBP)-2 (E18-P42), -5 (E16-P14), -7 (E12-P0), and -3 (E12-P0) were positively correlated with IGF-I, while IGFBP-3 (P0-P28) was negatively correlated with IGF-I. In comparison, IGF-IR (E18-P42), IGFBP-2 (E18-P42), IGFBP-5 (E14-P0), and IGFBP-3 (E16-P0) were positively correlated with IGF-II, while IGF-IR (E10-E16) and IGFBP-3 (P0-P28) were negatively correlated with IGF-II. Moreover, IGFBP-2 (E16-P42), -7 (E10-E16), and -3 (E10-E16) were positively correlated with IGF-IR, while IGFBP-3 (P0-P28) was negatively correlated with IGF-IR. Finally, IGFBP-7 (E12-P0) was positively correlated with IGFBP-3, while IGFBP-2 (P0-P28) and -7 (P0-P42) were negatively correlated with IGFBP-3. Overall, the AA chickens exhibited higher levels of IGF-I, IGF-IR, and IGFBP-2 mRNA expression than the LL chickens, while the opposite was true for IGFBP-7. No strain differences in IGF-I, IGF-IR, and IGFBP-7 mRNA expression were detected between LA and AA chickens; however, a strain difference was observed for IGFBP-2. LA chickens exhibited higher levels of IGFBP-2 than LL chickens, while the opposite was true for IGFBP-7. Our data show the first evidence that certain genes may be correlated during specific developmental periods and that strain differences in the expression of those genes in LS and AA chickens are due to differential responses to the same diet.

Keywords

References

  1. Akaogi, K., J. Sao, Y. Okabe, Y. Sakamoto, H. Yasumitsu and K. Miyazaki. 1996. Synergistic growth stimulation of mouse fibroblasts by tumor-derived adhesion factor with insulin-like growth factors and insulin. Cell Growth Differ. 7:1671-1677 https://doi.org/10.1095/biolreprod.106.058867
  2. Bacon, W. L., K. E. Nestor, D. A. Emmerson, R. Vasilatos-Younken and D. W. Long. 1993. Circulating IGF-I in plasma of growing male and female turkeys of medium and heavy weight lines. Domest. Anim. Endocrinol. 10(4):267-77 https://doi.org/10.1016/0739-7240(93)90031-6
  3. Baxter, R. C. and J. L. Martin. 1989. Structure of the Mr 140-000 growth hormone-dependent insulin-like growth factor binding protein complex: Determination by reconstitution and affinity labeling. Proc. Natl. Acad. Sci. USA 86:6898-6902 https://doi.org/10.1073/pnas.86.18.6898
  4. Beccavin, C., B. Chevalier, J. Simon and M. J. Duclos. 1999. Circulating insulin-like growth factors (IGF-I and -II) and IGF binding proteins in divergently selected fat or lean chickens: effect of prolonged fasting. Growth Horm. IGF Res. 9:187-194
  5. Beccavin, C., B. Chevalier, L. A. Cogburn, J. Simon and M. J. Duclos. 2001. Insulin-like growth factors and body growth in chickens divergently selected for high or low growth rate. J. Endocrinol. 168:297-306 https://doi.org/10.1677/joe.0.1680297
  6. Beebe, D. C., M. H. Silver, K. S. Belcher, J. J. van Wyk, M. E. Svoboda and P. S. Zelenka. 1987. Lentropin, a protein that controls lens fiber formation, is related functionally and immunologically to the insulinlike growth factors. Proc. Nat1. Acad. Sci. USA 84:2327-2330 https://doi.org/10.1073/pnas.84.8.2327
  7. Buyse, J. and E. Decuypere. 1999. The role of the somatotrophic axis in the metabolism of the chicken. Domest. Anim. Endocrinol. 17(2-3):245-255 https://doi.org/10.1016/S0739-7240(99)00041-7
  8. Cerro, J. A., A. Grewal, T. L. Wood and J. E. Pintar. 1993. Tissuespecific expression of the insulin-like growth factor-binding protein (IGFBP) mRNAs in mouse and rat development. Regul. Pept. 48:189-198 https://doi.org/10.1016/0167-0115(93)90347-B
  9. Cheng, C. M., B. Kelley, J. Wang, D. Strauss, D. A. Eagles and C. A. Bondy. 2003. A ketogenic diet increases brain insulin-like growth factor receptor and glucose transporter gene expression. Endocrinology 144(6):2676-2682 https://doi.org/10.1210/en.2002-0057
  10. Clemmons, D. R. 1998. Role of insulin-like growth factor binding proteins in controlling IGF actions. Mol. Cell. Endocrinol. 140:19-24 https://doi.org/10.1016/S0303-7207(98)00024-0
  11. Clemmons, D. R., M. L. Deboff, W. H. Busby, M. L. Bayne and M. A. Cascieri. 1992. Competition for binding to insulin-like growth factor (IGF) binding protein-2, 3, 4, and 5 by the IGFs and IGF analogs. Endocrmology 131(2):890-895 https://doi.org/10.1210/en.131.2.890
  12. Conlon, M. A. and K. Kita. 2002. Muscle protein synthesis rate is altered in response to a single injection of insulin-like growth factor-I in seven-day-old Leghorn chicks. Poult. Sci. 81(10):1543-1547
  13. Duclos, M. J., R. S. Wilkie and C. Goddard. 1991. Stimulation of DNA synthesis in chicken muscle satellite cells by insulin and insulin-like growth factors: evidence for exclusive mediation by a type-I insulin-like growth factor receptor. J. Endocrinol. 128:35-42 https://doi.org/10.1677/joe.0.1280035
  14. Ernst, C. W., D. C. McFarland and M. E. White. 1996. Expression of insulin-like growth factor II (IGF-II), IGF binding protein-2 and myogenin during differentiation of myogenic satellite cells derived from the turkey. Differentiation 61(1):25-33 https://doi.org/10.1046/j.1432-0436.1996.6110025.x
  15. Fliesen, T., D. Maiter, G. Gerard, L. E. Undewood, M. Maes and J. M. Ketelsleger. 1989. Reduction of serum insulin-like growth factor-I by dietary restriction is age dependent. Pediatr. Res. 26:415-419 https://doi.org/10.1203/00006450-198911000-00010
  16. Florini, J. R., D. Z. Ewton and S. L. Roof. 1991. Insulin-like growth factor-I stimulates terminal myogenic differentiation by induction of myogenin gene expression. Mol. Endocrinol. 5(5):718-724 https://doi.org/10.1210/mend-5-5-718
  17. Gabillard, J. C., B. B. Kamangar and N. Montserrat. 2006. Coordinated regulation of the GH/IGF system genes during refeeding in rainbow trout (Oncorhynchus mykiss). J. Endocrinol. 191(1):15-24 https://doi.org/10.1677/joe.1.06869
  18. Gautsch, T. A., S. M. Kandl, S. M. Donovan and D. K. Layman. 1998. Response of the IGF-I system to prolonged undernutrition and its involvement in somatic and skeletal muscle growth retardation in rats. Growth Dev. Aging. Spring-Summer 62(1-2):13-25
  19. Gerrard, D. E. and A. L. Grant. 1994. Insulin-like growth factor-II expression in developing skeletal muscle of double muscled and normal cattle. Domest. Anim. Endocrinol. 11(4):339-347 https://doi.org/10.1016/0739-7240(94)90005-1
  20. Gerrard, D. E., C. S. Okamura and A. L. Grant. 1999. Expression and location of IGF binding proteins-2, -4, and -5 in developing fetal tissues. J. Anim. Sci. 77:1431-1441
  21. Gerrard, D. E., C. S. Okamura, M. A. Ranalletta and A. L. Grant. 1998. Developmental expression and location of IGF-I and IGF-II mRNA and protein in skeletal muscle. J. Anim. Sci. 76(4):1004-1011
  22. Girbau, M., J. A. Gomez, M. A. Lesniak and F. De Pablo. 1987. Insulin and insulin-like growth factor I both stimulate metabolism, growth and differentiation in the postneurula chick embryo. Endocrinology 121:1477-1482 https://doi.org/10.1210/endo-121-4-1477
  23. Green, B. N., S. B. Jones, R. D. Streck, T. L. Wood, P. Rotwein and J. E. Pintar. 1994. Distinct expression patterns of insulinlike growth factor binding proteins 2 and 5 during fetal and postnatal development. Endocrinology 134(2):954-962 https://doi.org/10.1210/en.134.2.954
  24. Guernec, A., B. Chevalier and M. J. Duclos. 2001. Effects of nutritional state and genotype on IGF-I and myostatin mRNA levels in chicken muscle. Br. Poult. Sci. 42:S25-S26
  25. Hoeflich, A., L. Bünger, S. Nedbal, U. Renne, M. W. Elmlinger, W. F. Blum, C. Bruley, H. J. Kolb and E. Wolf. 2004. Growth selection in mice reveals conserved and redundant expression patterns of the insulin-like growth factor system. Gen. Comp. Endocrinol. 136(2):248-259 https://doi.org/10.1016/j.ygcen.2003.12.019
  26. Hua, K. M., R. Ord, S. Kirk, Q. J. Li, S. C. Hodgkinson, G. S. Spencer, P. C. Molan and J. J. Bass. 1993. Regulation of plasma and tissue levels of insulin-like growth factor-I by nutrition and treatment with growth hormone in sheep. J. Endocrinol. 136:217-224 https://doi.org/10.1677/joe.0.1360217
  27. Huybrechts, L. M., D. B. King, T. J. Lauterio, J. Marsh and C. G. Scanes. 1985. Plasma concentrations of somatomedin-C in hypophysectomized, dwarf and intact growing domestic fowl as determined by heterologous radioimmunoassay. J. Endocrinol. 104(2):233-239 https://doi.org/10.1677/joe.0.1040233
  28. Hwa, V., C. Tomasini-Sprenger, A. L. Bermejo, R. G. Rosenfeld and S. R. Plymate. 1998. Characterization of insulin-like growth factor-binding protein-related protein-1 in prostate cells. Journal of Clinical Endocrinology and Metabolism 83:4355-4362 https://doi.org/10.1210/jc.83.12.4355
  29. Hwa, V., Y. Oh and R. G. Rosenfeld. 1999. The insulin-like growth factor-binding protein (IGFBP) superfamily. Endocr. Rev. 20(6):761-787 https://doi.org/10.1210/er.20.6.761
  30. James, P. L., S. B. Jones, W. H. Busby, D. R. Clemmons and P. Rotwein. 1993. A highly conserved insulin-like growth factorbinding protein (IGFBP-5) is expressed during myoblast differentiation. J. Biol. Chem. 268:22305-22312 https://doi.org/10.1073/pnas.0400230101
  31. Jones, J. I. and D. R. Clemmons. 1995. Insulin-like growth factors and their binding proteins: biological actions. Endocr. Rev. 16:3-34
  32. Kato, M. V., H. Sato, T. Tsukada, Y. Ikawa, S. Aizawa and M. Nagayoshi. 1996. A follistatin-like gene, mac25, may act as a growth suppressor of osteosarcoma cells. Oncogene 12:1361-1364
  33. Kikuchi, K., F. C. Buonomo, Y. Kajimoto and P. Rotwein. 1991. Expression of insulin-like growth factor I during chicken development. Endocrinology 128:1323-1328 https://doi.org/10.1210/endo-128-3-1323
  34. Kita, K., F. M. Tomas, P. C. Owens, S. E. Knowles, B. E. Forbes, Z. Upton, R. Hughes and F. J. Ballard. 1996. Influence of nutrition on hepatic IGF-I mRNA levels and plasma concentrations of IGF-I and IGF-II in meat-type chickens. J. Endocrinol. 149:181-190 https://doi.org/10.1677/joe.0.1490181
  35. Kita, K., K. Nagao and J. Okumura. 2005. Nutritional and tissue specificity of IGF-I and IGFBP-2 gene expression in growing chickens. Asian-Aust. J. Anim. Sci. 18(5):747-754
  36. Kita, K., K. Nagao, N. Taneda, Y. Inagaki, K. Hirano, T. Shibata, M. A. Yaman, M. A. Conlon and J. Okumura. 2002. Insulin-Like Growth Factor Binding Protein-2 gene expression can be regulated by diet manipulation in several tissues of young chickens. J. Nutr. 132:145-151
  37. Kita, K., T. Shibata, M. Aman Yaman, K. Nagao and J. Okumura. 2002. Response of muscle protein synthesis to the infusion of insulin-like growth factor-I and fasting in young chickens. Asian-Aust. J. Anim. Sci. 15(12):1760-1764
  38. Lee, H. G., Y. J. Choi, S. R. Lee, H. Kuwayama, H. Hidari and S. K. You. 2005. Effects of dietary protein and growth hormonereleasing peptide (GHRP-2) on plasma IGF-1 and IGFBPs in Holstein steers. Domest. Anim. Endocrinol. 28:134-146 https://doi.org/10.1016/j.domaniend.2004.07.001
  39. Leili, S., F. C. Buonomo and C. G. Scanes. 1997. The effects of dietary restriction on insulin-like growth factor (IGF)-I and II, and IGF-binding proteins in chickens. Proc. Soc. Exp. Biol. Med. 216:104-111 https://doi.org/10.1016/S0305-0491(99)00134-0
  40. Listrat, A., D. E. Gerrard, N. Boulle, A. Groyer and J. Robelin. 1994. In situ localization of muscle insulin-like growth factor-II mRNA in developing bovine fetuses. J. Endocrinol. 140(2):179-187 https://doi.org/10.1677/joe.0.1400179
  41. Lowe, W. L. Jr, M. Adamo, H. Werner, C. T. Roberts Jr and D. LeRoith. 1989. Regulation by fasting of rat insulin-like growth factor I and its receptor. Effects on gene expression and binding. J. Clin. Invest. 84:619-626 https://doi.org/10.1172/JCI114207
  42. Matsumura, Y., M. Domeki, K. Sugahara, T. Kubo, C. T. Roberts Jr, D. LeRoith and H. Kato. 1996. Nutritional regulation of insulin-like growth factor-I receptor mRNA levels in growing chickens. Biosci. Biotechnol. Biochem. 60(6):979-982 https://doi.org/10.1271/bbb.60.979
  43. McMurtry, J. P., G. L. Francis and Z. Upton. 1997. Insulin-like growth factors in poultry. Domest. Anim. Endocrinol. 14(4):199-229 https://doi.org/10.1016/S0739-7240(97)00019-2
  44. Ning, Y., A. G. Schuller, S. Bradshaw, P. Rotwein, T. Ludwig, J. Frystyk and J. E. Pintar. 2006. Diminished growth and enhanced glucose metabolism in triple knockout mice containing mutations of insulin-like growth factor binding protein-3, -4, and -5. Mol. Endocrinol. 20(9):2173-2186 https://doi.org/10.1210/me.2005-0196
  45. Oh, Y., S. R. Nagalla, Y. Yamanaka, H. S. Kim, E. Wilson and R. G. Rosenfeld. 1996. Synthesis and characterization of insulinlike growth factor-binding protein (IGFBP)-7. J. Biological Chem. 271:30322-30325 https://doi.org/10.1074/jbc.271.48.30322
  46. Orlowski, C. C., A. L. Brown, G. T. Ooi, Y. W. Yang, L. Y. Tseng and M. M. Rechler. 1990. Tissue, developmental, and metabolic regulation of messenger ribonucleic acid encoding a rat insulin-like growth factor-binding protein. Endocrinol. 126(1):644-652 https://doi.org/10.1210/endo-126-1-644
  47. Oster, M. H., N. Levin, P. J. Fielder, I. C. A. Robinson, R. C. Baxter and M. J. Cronin. 1996. Developmental differences in the IGF-I system response to severe and chronic caloric malnutrition. Am. J. Physiol. 270:E646-653
  48. Pym, R. A., R. J. Johnson, D. B. Etse and P. Eason. 1991. Inheritance of plasma insulin-like growth factor-I and growth rate, food intake, food efficiency and abdominal fatness in chickens. Br. Poult. Sci. 32(2):285-293 https://doi.org/10.1080/00071669108417352
  49. Rotwein, P. 1991. Structure, evolution, expression and regulation of insulin-like growth factors I and II. Growth Factors 5(1):3-18 https://doi.org/10.3109/08977199109000267
  50. Sanchez-Gomez, M., K. Malmlof, W. Mejia, A. Bermudez, M. T. Ochoa, S. Carrasco-Rodríguez and A. Skottner. 1999. Insulinlike growth factor-I, but not growth hormone, is dependent on a high protein intake to increase nitrogen balance in the rat. Br. J. Nutr. 81:145-152 https://doi.org/10.1017/S0007114599000288
  51. Scanes, C. G., E. A. Dunnington, F. C. Buonomo, D. J. Donoghue and P. B. Siegel. 1989. Plasma concentrations of insulin like growth factors (IGF-)I and IGF-II in dwarf and normal chickens of high and low weight selected lines. Growth Dev. Aging 53:151-157
  52. Schmid, C., T. Steiner and E. R. Froesch. 1983. Preferential enhancement of myoblast differentiation by insulin-like growth factors (IGF-I and IGF-II) in primary cultures of chicken embryonic cells. FEBS Lett. 161:117-121 https://doi.org/10.1016/0014-5793(83)80742-X
  53. Severgnini, S., D. T. Lowenthal, W. J. Millard, F. A. Simmen, B. H. Pollock and S. E. Borst. 1999. Altered IGF-I and IGFBPs in senescent male and female rats. J. Gerontol. A Biol. Sci. Med. Sci. 54(3):B111-115 https://doi.org/10.1093/gerona/54.3.B111
  54. Spangenburg, E. E., T. Abraha, T. E. Childs, J. S. Pattison and F. W. Booth. 2003. Skeletal muscle IGF-binding protein-3 and -5 expressions are age, muscle, and load dependent. Am. J. Physiol. Endocrinol. Metab. 284(2):E340-350
  55. Sun, Z. H., Z. L. Tan, J. H. Yao, Z. R. Tang, J. G. Shan, J. P. Hu, S. X. Tang and Y. M. Jiang. 2007. Effects of intra-duodenal infusion of limiting amino acids on plasma insulin-like growth factor I, growth hormone, insulin and liver insulin-like growth factor I mRNA in growing goat fed a maize stover-based diet. Asian-Aust. J. Anim. Sci. 20(5):733-741
  56. Tesseraud, S., R. A. E. Pym, E. Le Bihan-Duval and M. J. Duclos. 2003. Response of broilers selected on carcass quality to dietary protein supply: Live performance, muscle development, and circulating insulin-like growth factors (IGF-I and -II). Poult. Sci. 82:1011-1016
  57. Thissen, J. P., J. M. Ketelslegers and L. E. Underwood. 1994. Nutritional regulation of the insulin-like growth factors. Endocrinol. Rev. 15:80-101
  58. Tollefsen, S., R. Lajara, R. McCusker, D. Clemmons and P. Rotwein. 1989. Insulin-like growth factors in muscle development: expression of IGF-I and the IGF receptor and IGF binding protein during myoblast differentiation. J. Biol. Chem. 264:13810-13817
  59. Trouten-Radford, L., X. Zhao and B. W. McBride. 1991. IGF-I receptors in embryonic skeletal muscle of three strains of chickens selected for differences in growth capacity. Domest. Anim. Endocrinol. 8(1):129-137 https://doi.org/10.1016/0739-7240(91)90047-N
  60. Vestergaard, M., S. Purup, J. Frystyk, P. L$\phi$vendahl, M. T. S$\phi$rensen, P. M. Riis, D. J. Flint and K. Sejrsen. 2003. Effects of growth hormone and feeding level on endocrine measurements, hormone receptors, muscle growth and performance of prepubertal heifers. J. Anim. Sci. 81:2189-2198
  61. Yun, J. S., D. S. Seo, W. K. Kim and Y. Ko. 2005. Expression and relationship of the insulin-like growth factor system with posthatch growth in the Korean Native Ogol chicken. Poult. Sci. 84(1):83-90
  62. Zadeh, S. M. and M. Binoux. 1997. The 16-kDa proteolytic fragment of insulin-like growth factor (IGF) binding protein-3 inhibits the mitogenic action of fibroblast growth factor on mouse fibroblasts with a targeted disruption of the type 1 IGF receptor gene. Endocrinol. 138(7):3069-3072 https://doi.org/10.1210/en.138.7.3069

Cited by

  1. Effects of dietary methionine on breast muscle growth, myogenic gene expression and IGF-I signaling in fast- and slow-growing broilers vol.7, pp.1, 2017, https://doi.org/10.1038/s41598-017-02142-z
  2. Molecular characterization and expression profiling of BMP 3 gene in broiler and layer chicken vol.45, pp.4, 2018, https://doi.org/10.1007/s11033-018-4184-x
  3. Delayed access to feed alters gene expression associated with hormonal signaling, cellular differentiation, and protein metabolism in muscle of newly hatch chicks vol.292, pp.None, 2009, https://doi.org/10.1016/j.ygcen.2020.113445